Exploring public interest in gut microbiome dysbiosis, NAFLD, and probiotics using Google Trends

Scientific interest related to the role of gut microbiome dysbiosis in the pathogenesis of non-alcoholic fatty liver disease (NAFLD) has now been established and is constantly growing. Therefore, balancing dysbiosis, through probiotics, would be a potential therapy. In addition to scientific interest, on the other hand, it is important to evaluate the interest in these topics among the population. This study aimed to analyze, temporally and geographically, the public's interest in gut microbiome dysbiosis, NAFLD, and the use of gut probiotics. The most widely used free tool for analyzing online behavior is Google Trends. Using Google Trends data, we have analyzed worldwide volume searches for the terms “gut microbiome”, “dysbiosis”, “NAFLD” and “gut probiotic” for the period from 1, January 2007 to 31 December 2022. Google's relative search volume (RSV) was collected for all terms and analyzed temporally and geographically. The RSV for the term “gut microbiome” has a growth rate of more than 1400% followed, by “gut probiotics” (829%), NAFLD (795%), and “dysbiosis” (267%) from 2007 to 2012. In Australia and New Zealand, we found the highest RSV score for the term “dysbiosis” and “gut probiotics”. Moreover, we found the highest RSV score for the term “NAFLD” in the three countries: South Korea, Singapore, and the Philippines. Google Trends analysis showed that people all over the world are interested in and aware of gut microbiome dysbiosis, NAFLD, and the use of gut probiotics. These data change over time and have a geographical distribution that could reflect the epidemiological worldwide condition of NAFLD and the state of the probiotic market.

The purpose of our study is to analyze, temporally and geographically, the public's interest related to gut microbiome dysbiosis, NAFLD, and the use of gut probiotics using Google Trends data, so that physicians and researchers should not only be aware of the hotspots of scientific research but also of the concerns of public interest.

Relative search volume (RSV) trend
Figure 1 depicts the overall global RSV trends for all four searched terms from 2007 to 2022.RSV grew from 45 to about 293.There was a small negative decline between 2008 and 2012.Despite minor fluctuations, the average search strength demonstrated an overall upward tendency.The curve started to rise again in 2013.
Among the four searched terms, "gut microbiome" and "gut probiotics", changed respectively from an RSV of 6 and 7.4 to an RSV of 86.3 and 61.2.While "dysbiosis" and "NAFLD" have respectively an increase from 19.9 and 11.7 to 53.2 and 92.8 (Fig. 2).
When comparing the RSV value for the year 2022 to the value for the year 2007 for all four words (Fig. 3), the term "gut microbiome" shows a growth of about 1400%, followed by "gut probiotics" (829%), NAFLD (795%), and "dysbiosis" with 267%.

Country relative search volume (RSV) distribution
The geographic distribution graph for each searched term from 2007 to 2022 is shown in Fig. 4, while Table 1 shows the country RSV value for searched terms.
The top ten countries with the highest RSV for the term "gut microbiome" are Australia (RSV = 100), Ireland  On the other hand, concerning countries exhibiting the lowest RSV for the term "gut microbiome," the five ranked in ascending order are Russia (RSV = 4), Turkey (RSV = 4), Brazil (RSV = 6), Mexico (RSV = 6) and Poland (RSV = 6).

Relative search volume (RSV) of associated queries
The top ten queries related to the searched terms from 2007 to 2022 are listed in Table 2.

Discussion
Nowadays, open data from the internet is being used more and more in health research.Understanding and monitoring public perceptions of disease management and treatment are equally crucial.Google Trends is rapidly becoming the most popular tool for recognizing internet activity 34 .In our study using Google search traffic data, we observed public interest and knowledge consisting of annual trends, geographic distribution and related topics related to gut microbiome dysbiosis, NAFLD, and the usage of gut probiotics.RSV annual trend showed an overall increasing trend, although with slight fluctuation, and a decline in RSV from years 2008 to 2012 (Fig. 1).The increase is higher, especially in the last year, with an RSV that varies from a value of 224.9 to a value of 293.3.
Observing the distinct search terms, we could find that those with a considerable increase in RSV values are those related to the terms "gut microbiome", followed by "gut probiotics", "NAFLD" and finally "dysbiosis" (Fig. 2).
These trends over time reflect the growing research interest in the dysbiosis of the gut microbiome, its role in several diseases including NAFLD and the interest in gut probiotics as a therapy to restore dysbiosis.
In recent years, the demand for probiotic bacteria-containing products has increased.More and more people are adding probiotic bacteria to their diets as functional food supplements because of the positive effects they have on health [35][36][37] .When it comes to functional food ingredients, probiotics are by far the most popular choice.Studies have shown that probiotic strains can help treat a number of illnesses, including gastrointestinal distress, bacterial vaginosis, and urinary tract infections [38][39][40] .Protection from dangerous bacteria in the digestive tract, better bowel movement, reduced cholesterol levels, relief from lactose intolerance and inflammation, and so on are just some of the health benefits associated with probiotics 41,42 .
Another interesting finding in this study was the variation in interest in the searched terms across countries (Fig. 4 and Table 1).
Interestingly, in Australia, and New Zealand, we found the highest RSV score for the term "dysbiosis" and "gut probiotics".Australia is also in the first rank for the term "gut microbiome".
From 2021 to 2030, the worldwide probiotics industry is anticipated to increase from 2021's valuation of about USD 58 billion with a CAGR (compound annual growth rate) of 7.5% 43,44 .Rising public interest in preventative Table 2.The most used related topics for the period 2007-2022, from Google Trends.Users who searched for the terms "gut microbiome", "dysbiosis", "NAFLD", and "gut probiotics", also searched for these topics.The score is on a relative scale: 100 indicates the most searched query, and 50 indicates a query with half the searches compared to the most searched query; RSV = relative search volume; data accessed on January 18, 2023.www.nature.com/scientificreports/medicine and the refinement of highly effective probiotic strains are driving the industry.When taken in sufficient quantities, probiotics have positive benefits on the body, including enhanced gastrointestinal wellness and decreased intestinal inflammation 45,46 .By bolstering the immune system, probiotics play an important role in preventing the onset of illness 45,46 .Hence, increasing focus on preventative medicine is anticipated to fuel market expansion throughout the forecast period.More than 40.0% of worldwide probiotic market revenue was generated in the Asia Pacific area in 2021 43,44 .Increased consumer awareness is largely attributed to the competitive strategies implemented by multinational companies in the region.Market expansion in the region is anticipated to be driven by a number of factors, including a rising population, rising disposable income, and an increasing standard of life 43,44,47 .The association between RSV and the topic of probiotics and dysbiosis might be caused by the recommendations of probiotics to restore the gut microbiome 12,46 .
As far as the "NAFLD" term we found the highest RSV score in the three countries: South Korea, Singapore and the Philippines.An estimated 32.4% of the world's population has NAFLD, and that number has been steadily rising over the past decade 48 .Among Asian countries, NAFLD is more recent (27%), compared to Europe and North America (24%) 49 .From 5% in Singapore to 30% in Indonesia, the prevalence of NAFLD in Asia substantially varies 50,51 .The prevalence of metabolic diseases is on the rise in Korea, from 24.9% in 1998 to 29.0% in 2013 52 .This has become a major public health issue 50,51 .In Singapore, the number of people living with NAFLD is expected to increase from 1,492,000 in 2019 to 1,799,000 in 2030 53 .In addition, it is concerning that at least one-third of the general population in the Philippines has NAFLD; the prevalence rate is 38%, compared to 25% globally 54 .It is believed that the rising prevalence of NAFLD in the Asia-Pacific area is due to the widespread adoption of Western food and lifestyle practices and predisposing genetic factors among many different communities 55 .Rapid industrialization in many Asian nations has led to a shift toward sedentary behaviors and overnutrition, both of which are strongly linked to metabolic problems 56 .Moreover, despite the fact that obesity and diabetes are well-known risk factors for the disease 57,58 , a sizable population in the Asian region suffers from NAFLD while having a healthy weight 59 .It is expected that the number of people diagnosed with NAFLD and NASH throughout Asia will continue to rise, especially in rapidly aging populations, who are more likely to develop chronic lifestyle-related illnesses 60 .
The top ten related queries in terms of searches from 2007 to 2022 are listed in Table 2.The queries related to the term "gut microbiome", are related to understanding by the public of what the gut microbiome is, what bacteria it consists of, how to diagnose gut dysbiosis, and how to keep it healthy through diet, food, and also probiotics.In addition, some search terms refer to the link between the gut and brain, the so-called gut-brain axis.The gut-liver axis is increasingly being recognized as the underlying cause of NAFLD 14,16,17 .By dysregulating the gut-liver axis, gut microbiome dysbiosis, which contributes to the development of NAFLD, promotes an increase in intestinal permeability and uncontrolled transport of microbial metabolites into the liver 14,16,17 .Moreover, NAFLD is facilitated by a dysfunctional gut-liver axis, which affects hepatocyte lipid and glucose metabolism and disturbs the equilibrium of inflammatory mediators 14,16,17 .
The public queries related to the term "dysbiosis" are related to its definition, the pathogenetic mechanisms that underlie it, possible diagnosis, and treatment.
The queries related to the term "NAFLD" are related to its definition and pathogenetic mechanisms, the correlation with non-alcoholic steatohepatitis (NASH), the diagnosis of fibrosis, and care through diet.Research has connected dysbiosis in the gut microbiome not only to the development of NAFLD but also to its progression in NASH, which is characterized histologically by hepatocyte damage and various degrees of fibrosis, up until cirrhosis [6][7][8]13 .
The queries related to the terms "gut probiotics" are related to the public's search for an "effective" probiotic treatment.Among related queries to "gut probiotics" appear also the terms "leaky" or "probiotics for the leaky gut".The intestinal barrier permits communication between the digestive tract and the liver 61,62 .Tight connections between intestinal cells are essential for maintaining the integrity of the intestinal barrier 63 .A leaky gut, defined by decreased intestinal barrier function, is a well-established characteristic of dysbiosis in NAFLD patients 64,65 .Dysbiosis and associated reduced gut permeability results in an increase in gut-derived toxins in the systemic circulation, constituting metabolic endotoxemia, which contributes to the development of the persistent low-grade inflammation observed in NAFLD 65,66 .
In conclusion, Google Trends analysis showed that people all over the world are interested in and aware of gut microbiome dysbiosis, NAFLD, and the use of gut probiotics.These data change over time and have a geographical distribution that could reflect the epidemiological worldwide condition of NAFLD and the state of the probiotic market.The collection of such information has the potential to improve the monitoring of numerous diseases in the future.A number of variables limit Google Trends' applicability.Because Google Trends removes queries from the same person over a short time period to reduce counts of continued searching, the service may suffer from sampling bias.Google's search algorithms are constantly being improved, so the same query terms may provide different results.This will make it more challenging to replicate these studies, which rely on reproducible results.Whether or not people learn more about health issues as a result of using Google to research them is debatable.This is because Google Trends only reports how often a term has been searched without providing any information on the quality of the results that may be used to gauge how much useful information can be gleaned from them.Another limitation that could affect our analysis is that the internet is becoming increasingly widespread, embracing an increasingly wide range of populations.Now, you can access the internet with different devices, such as smartphones.

Methods
Data from Google Trends is expressed as relative search volume (RSV).The RSV is presented on a standardized scale from 0 (no search interest) to 100 (greatest search interest).We have searched worldwide RSV for the English terms "gut microbiome, "dysbiosis", "NAFLD" and "gut probiotics".The search was limited to the period from 1 January 2007 to 31 December 2022.Data related to the public interest was downloaded in "csv" format from the Google Trends website 34 on January 18, 2023.Since the data fluctuates over time, we have processed the data, which is shown as an annual average of the monthly values of RSV from 1 January 2007 to 31 December 2022.Our analysis used the country option to determine the geographical distribution of RSV for each searched term.Google Trends can also identify searches that are connected to a given search term and categorize these searches as "queries." The top searches option displays popular search phrases that are comparable to the keyword input, during a specific time period.We analyze the 'top' searches for each term "gut microbiome, "dysbiosis", "NAFLD" and "gut probiotics".

Figure 1 .
Figure 1.World annual mean trend of the RSV (relative search volume) from January 2007 until December 2022 (15 years), given by the sum of the mean RSV value of each searched term from Google Trends, data accessed on January 18, 2023.

Figure 3 .
Figure 3.The ratio (%) between the RSV (relative search volume) value of the year 2022 and the value of the year 2007 for the searched terms: "gut microbiome, "dysbiosis", "NAFLD" and "gut probiotics.

Figure 4 .
Figure 4. Geographic distribution of the RSV (relative search volume) for the searched terms from Google Trends: "gut microbiome" is colored in blue, "dysbiosis" is colored in red, "NAFLD" is colored in yellow, and "gut probiotics" is colored in green.The color gradient is proportional to the value of RSV; data accessed on January 18, 2023. https://doi.org/10.1038/s41598-023-50190-5www.nature.com/scientificreports/